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A non-trophic interaction chain links predators in different spatial niches


Non-trophic interactions, driven by one species changing the behavior but not density of another species, appear to be as pervasive as those involving consumption. However, ecologists have only begun to explore non-trophic interactions in species-rich communities. We investigated interactions within a community including two predator–prey linkages separated in space: ground-active predatory beetles and their fly egg prey on the ground, and lady beetles and their aphid prey in plant foliage. In field and greenhouse experiments we found that ground-active predators preyed heavily on fly eggs except when both aphids and lady beetles were present. The aphids drop from the foliage to escape foraging lady beetles, and once on the ground apparently triggered ground-active predators to switch from attacking fly eggs to attacking aphids. This suggests that the first non-trophic interaction in the foliage, mediated by aphid antipredator behavior, in turn initiated and accentuated a second non-trophic interaction on the ground, mediated by prey-switching behavior by ground predators. Our results demonstrate that successive non-trophic interactions can be propagated along chains of more than three species, and can serve to link species that are otherwise spatially isolated.

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  1. Borer ET, Anderson K, Blanchette CA, Broitman B, Cooper SD, Halpern BS, Seabloom EW, Shurin JB (2002) Topological approaches to food web analyses: a few modifications may improve our insights. Oikos 99:397–401

  2. Byrnes J, Stachowicz JJ, Hultgren KM, Hughes AR, Olyarkin SV, Thornber CS (2006) Predator diversity strengthens trophic cascades in kelp forests by modifying herbivore behaviour. Ecol Lett 9:61–71

  3. Cronin JT, Haynes KJ, Dillemuth T (2004) Spider effects on planthopper mortality, dispersal, and spatial population dynamics. Ecology 85:2134–2143

  4. Crowder LB, Squires DD, Rice JA (1997) Non-additive effects of terrestrial and aquatic predators on juvenile estuarine fish. Ecology 78:1796–1804

  5. Doane JF, Chapman RK (1962) Oviposition preference of the cabbage maggot, Hylemya brassicae (Bouché). J Econ Entomol 55:137–138

  6. Goudard A, Loreau M (2008) Nontrophic interactions, biodiversity, and ecosystem functioning: an interaction web model. Am Nat 171:91–106

  7. Grabowski JH, Kimbro DL (2005) Predator-avoidance behavior extends trophic cascades to refuge habitats. Ecology 86:1312–1319

  8. Halaj J, Wise DH (2001) Terrestrial trophic cascades: how much do they trickle? Am Nat 157:262–281

  9. Harmon JP, Andow DA (2004) Indirect effects between shared prey: predictions for biological control. Biocontrol 49:605–626

  10. Holt RD (1977) Predation, apparent competition, and the structure of prey communities. Theor Popul Biol 12:197–229

  11. Huang C, Sih A (1990) Experimental studies on behaviorally mediated indirect interactions through a shared predator. Ecology 71:1515–1522

  12. Knight TM, McCoy MW, Chase JM, McCoy KA, Holt RD (2005) Trophic cascades across ecosystems. Nature 437:880–883

  13. Lathrop RC, Johnson BM, Johnson TB, Vogelsang MT, Carpenter SR, Hrabik TR, Kitchell JF, Magnuson JJ, Rudstam LG, Stewart RS (2002) Stocking piscivores to improve fishing and water quality: a synthesis of the Lake Mendota biomanipulation project. Freshw Biol 47:2410–2424

  14. Letourneau DK, Dyer LA, Vega GC (2004) Indirect effects of a top predator on a rainforest understory plant community. Ecology 85:2144–2152

  15. Losey JE, Denno RF (1998) Positive predator-predator interactions: enhanced predation rates and synergistic suppression of aphid populations. Ecology 79:2143–2152

  16. Luttbeg B, Rowe L, Mangel M (2003) Prey state and experimental design affect relative size of trait- and density-mediated indirect effects. Ecology 84:1140–1150

  17. McAllister MK, Roitberg BD (1987) Adaptive suicidal behavior in pea aphids. Nature 328:797–799

  18. Prasad RP, Snyder WE (2004) Predator interference limits fly egg biological control by a guild of ground-active beetles. Biol Control 31:428–437

  19. Prasad RP, Snyder WE (2006a) Polyphagy complicates conservation biological control that targets generalist predators. J Appl Ecol 43:343–352

  20. Prasad RP, Snyder WE (2006b) Diverse trait-mediated indirect interactions in a multi-predator, multi-prey community. Ecology 87:1131–1137

  21. Preisser EL, Bolnick DI, Benard MF (2005) Scared to death? The effects of intimidation and consumption in predator–prey interactions. Ecology 86:501–509

  22. Raimondi PT, Forde SE, Delph LF, Lively CM (2000) Processes structuring communities: evidence for trait-mediated indirect effects through induced polymorphisms. Oikos 91:123–130

  23. Relyea RA, Yurewicz KL (2002) Predicting community outcomes from pairwise interactions: integrating density- and trait-mediated effects. Oecologia 131:569–579

  24. Schmitz OJ (2008) Predators avoiding predation. Proc Natl Acad Sci USA 105:14749–14750

  25. Schmitz OJ, Beckerman AP, O’Brien KM (1997) Behaviorally-mediated trophic cascades: the effect of predation risk on food web interactions. Ecology 78:1388–1399

  26. Schmitz OJ, Krivan V, Ovadia O (2004) Trophic cascades: the primacy of trait-mediated indirect interactions. Ecol Lett 7:153–163

  27. Shurin JB, Borer ET, Seabloom EW, Anderson K, Blanchette CA, Broitman B, Cooper SD, Halpern BS (2002) A cross-ecosystem comparison of the strength of trophic cascades. Ecol Lett 5:785–791

  28. Siddon CE, Witman JD (2004) Behavioral indirect interactions: multiple predator effects and prey switching in the rocky subtidal. Ecology 85:2938–2945

  29. Snyder WE, Snyder GB, Finke DL, Straub CS (2006) Predator biodiversity strengthens herbivore suppression. Ecol Lett 9:789–796

  30. Soluk DA, Collins NC (1988) Synergistic interactions between fish and stoneflies: facilitation and interference among stream predators. Oikos 52:94–100

  31. Tscharntke T (1992) Cascade effects among 4 trophic levels: bird predation on galls affects density-dependent parasitism. Ecology 73:1689–1698

  32. Werner EE, Peacor SD (2003) A review of trait-mediated indirect interactions in ecological communities. Ecology 84:1083–1100

  33. Werner EE, Peacor SD (2006) Lethal and nonlethal predator effects on a herbivore guild mediated by system productivity. Ecology 87:347–361

  34. Wise DH (1981) Seasonal and yearly patterns in the densities of darkling beetles in a montane community. Environ Entomol 10:350–358

  35. Wissinger SA, McGrady J (1993) Intraguild predation and competition among larval dragonflies: direct and indirect effects on shared prey. Ecology 74:207–218

  36. Wootton JT (2002) Indirect effects in complex ecosystems: recent progress and future challenges. J Sea Res 48:157–172

  37. Yodzis P (1988) The indeterminacy of ecological interactions as perceived through perturbation experiments. Ecology 69:508–515

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This work was supported by grants from the Organic Farming Research Foundation, the United States Department of Agriculture’s Western Sustainable Agriculture Research and Education program, and the Natural Resources Conservation Endowment at Washington State University. D. Finke, S. Steffan, G. Snyder, C. Straub and D. Gillespie provided valuable comments on preliminary drafts of the manuscript. This study complies with the current laws in the country in which it was performed.

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Correspondence to William E. Snyder.

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Communicated by Sven Bacher.

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Prasad, R.P., Snyder, W.E. A non-trophic interaction chain links predators in different spatial niches. Oecologia 162, 747–753 (2010). https://doi.org/10.1007/s00442-009-1486-7

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  • Predator–prey interactions
  • Antipredator behavior
  • Herbivores
  • Biodiversity
  • Biological control